Download Counseling about the HPV Vaccine: Desexualize, Educate, and

Tips for Clinicians
Counseling about the HPV Vaccine: Desexualize, Educate, and Advocate
Richard M. Grimes PhD a,*, Laura J. Benjamins MD, MPH b, Kendra L. Williams BS c
a
b
c
Department of Internal Medicine, The University of Texas Health Science Center at Houston, Houston, TX 77030
Department of Pediatrics, The University of Texas Health Science Center at Houston, Houston, TX 77030
Medical Student, The University of Texas Health Science Center at Houston, Houston, TX 77030
a b s t r a c t
Information is provided for clinicians who treat adolescents and adult women to use when counseling patients about human papillomavirus (HPV) vaccine. A literature search was done to determine: (1) reasons for refusal of the vaccine, including cost and concerns that
immunization against HPV will lead to promiscuity; (2) potential for non-sexual transmission of HPV; (3) non-genital locations of HPV; (4)
non-genital cancers associated with HPV.
Vaccines for Children Program and the Affordable Care Act eliminate many costs. Neither biological nor behavioral evidence supports the idea
that sexual behavior changes after immunization. HPV is transmitted from person to person by non-sexual routes including mother to child at
birth and apparently by touch after birth. HPV is persistent in the environment, including medical environments. It has been found on
apparently sterilized instruments used in vaginal exams. Pathogenic HPV has been recovered from breast tissue, sinonasal areas, and nipples as
well as from hair follicles on arms, legs, scalps, eyebrows, and pubic hair. Pathogenic HPV was found in 6.5% of the oral cavities of a random
sample of Americans. HPV is known to cause anal and oral cancers. It has also been associated with skin cancers, breast tumors, and prostate
cancers. It is not known if the vaccine is protective against these cancers, but it is useful to educate about these other routes of transmission and
non-genital HPV linked cancers so that patients/parents do not just focus on the sexual nature of the human papillomavirus.
Key Word: HPV vaccine
Introduction
In June of 2006, the Federal Drug Administration
approved a quadrivalent vaccine that protects against 4
strains of the human papillomavirus (HPV) for use among
women and girls between the ages of 9 and 26. This vaccine
offers protection against HPV types 6 and 11, which cause
genital warts, as well as types 16 and 18, which are known to
be oncogenic. The vaccine trials proved that this new
immunization was highly effective in preventing infection
with the 2 HPV strains known to cause approximately 70% of
cervical cancers.1 In 2009, a bivalent vaccine for types 16 and
18 was approved and the quadrivalent vaccine was approved
for use among males. Release of these vaccines sparked hope
that there would be rapid uptake and that a gradual decline
in the number women with cervical cancer would ensue. To
be most effective in preventing infection, the immunization
series should be initiated prior to sexual debut. Therefore,
the Advisory Committee on Immunization Practices (ACIP)
recommends the routine vaccination of all females with 3
doses of the vaccine starting at age 11 or 12. Given that, in the
United States, nearly 33% of 9th graders have already had sex,
and almost 9% had first intercourse before the age of 13, this
recommendation seemed more than reasonable.2 There was
also a recommendation that older girls and women aged 1326 should be immunized. This means that counseling
patients about the utility of the vaccine becomes the
* Address correspondence to: Richard M. Grimes PhD, Division of General Internal
Medicine. The University of Texas Health Science Center at Houston, MSB 1.122,
6431 Fannin, Houston, TX 77030.
E-mail address: [email protected] (R.M. Grimes).
1083-3188/$ - see front matter
http://dxdoi.org/10.1016/j.jpag.2013.04.002
province of pediatricians, gynecologists, and other physicians who see young female patients. Despite initial enthusiasm, the actual use of the vaccine in the United States has
been less than ideal. The Centers for Disease Control and
Prevention (CDC) estimated that by 2010 only 48.7% of
females aged 13-17 have received $1 dose of HPV and 32%
have received the necessary 3 doses.3 A study of Kaiser Permanente women over 17 years of age showed that they are
only about half as likely to receive the vaccine as younger
adolescent females while a national survey of women ages
18-24 indicated that only 9% had received 1 injection of the
vaccine.4,5 Uptake among male patients has also been low.
This poor response to the vaccine represents a major lost
opportunity to reduce the prevalence of pathogenic HPV
strains, as well as to decrease the chance of benefiting from
herd immunity.6 The potential impact of herd immunity
arising from the vaccine can be seen by a study from
Australia where a school based immunization program
resulted in 72% of 14-15-year-old and 66% of 16-17-year-old
girls being immunized by 2009.7 The study showed that
among patients under 21 who appeared at the major
sexually transmitted disease clinic in Melbourne, the rate of
genital warts declined in women from 18.6% to 1.9% and
from 22.9% to 2.9% among heterosexual men.8
Reasons for Poor Uptake
A number of reasons have been offered to explain the poor
uptake of receiving the vaccine. The vaccine is costly; an
estimated $350-500 for the 3 shot series.9 An example of the
impact of cost on uptake was demonstrated in a study that
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R.M. Grimes et al. / J Pediatr Adolesc Gynecol 26 (2013) 243e248
found girls with some form of health insurance were 3 times
more likely to receive the vaccine.10 However, cost should not
be an issue for the pediatric population because the vaccine is
covered by the Vaccines for Children Program, which
provides vaccines at no cost to children that are uninsured or
underinsured through age 18.11 While this may be a problem
for those over 18, this concern should be less of a problem as
the Affordable Care Act (also known as Obamacare) is
implemented. Under its provisions, the HPV vaccine will be
covered at no cost for insured women beginning in 2013.12
Failure to achieve high rates of immunization has also
been associated with physician knowledge and behaviors. A
2006 paper found that only 46% of the pediatricians
surveyed would recommend giving the HPV vaccine to their
female patients ages 10 to 12.13 This is consistent with
a 2009 survey of 287 pediatricians which found that only
47% of pediatricians reported that they always recommended the HPV vaccine to their 11 and 12-year-old
patients. The same survey showed that family practitioners
and obstetrician/gynecologists recommended it to this age
only 34% and 36% of their patients. Overall the 3 specialty
groups recommended the vaccine in all age groups # 53% of
their patients.14 This may be due to lack of physician
knowledge about the vaccine. In a 2009 survey on HPV
knowledge of 1300 obstetrician/gynecologists, over 95% of
whom said that they provided care to adolescent females,
the respondents were asked to answer 3 questions about
the HPV vaccine. These were “Gardasil protects against _
forms of HPV that cause _% of cervical cancer and _% of
genital warts.” Less than 30% of the respondents got all 3
questions correct and less than 50% correctly answered
either of the last 2 questions.15 (The correct answers were 4
types, 70% of cervical cancers, and 90% of genital warts).
Acceptability and Concerns
One barrier to HPV immunization may be parental
concerns about the vaccine, for both their sons and their
daughters. There is limited information about the acceptability of the vaccine for boys. Two small convenience
sample studies found that mothers are as likely to immunize their sons as they are their daughters.16,17 In contrast
there are a large number of studies of the reasons for and
against taking the vaccine in adolescent females. In most
cases, the decision to vaccinate adolescents is made by
mothers. This decision to approve HPV immunization has
been shown to be connected to the mother’s attitudes and
behaviors. Sadigh et al18 found that women who had more
lifetime male sexual partners were over 3 times more likely
have their daughters immunized. There were also attitudinal enablers and barriers to mothers having their
daughters immunized. Low levels of religiosity and
a mother’s acceptance of premarital sex among 18-yearolds were correlated with their daughters being immunized.19 Several studies have revealed that some parents are
concerned that their daughters will become promiscuous if
they receive the vaccine.19-21 This fear seems to be linked to
religiosity; parents with frequent attendance at religious
services were 3 times more likely than parents who do not
attend services to have decided against vaccination.22 In
Calgary, Canada, the archbishop of the Catholic diocese has
forbidden requiring the vaccine in Catholic schools because
of this concern. While elsewhere in Canada, 70%-75% of teen
girls are immunized, only 18.9% of Catholic school girls in
Calgary have received the vaccine.23 In addition some
mothers are concerned that having their daughters immunized will be interpreted as giving their daughters
permission to have sex or to practice unsafe sex.24,25 In
some ways, this opposition is understandable in that most
of the professional and public discussion of the need for the
vaccine has been based on its protection against sexually
transmitted diseases and on making certain that children
receive the vaccine before sexual debut.26,27
The studies on the impact of attitudes and behaviors of
unimmunized individuals as they reach adulthood show
that they have a number of concerns. In 1 study of 244
women between 18 and 24 years of age found that unimmunized women cited concerns about cost of the vaccine
(27% of the sample), vaccine safety (22%), not needing the
vaccine because they were not sexually active (19%),
uncertainty about the effectiveness of the vaccine (16%),
and my doctor does not think that it is needed (7%). Interestingly, 87% of the women said that they would take the
vaccine if their doctor recommended it.5 This suggests an
important educational and advocacy role for gynecologists
as young women transition from pediatric care to adult care
and become the decision makers about their own care.
The sexualization of the vaccine has created difficulties
for providers in convincing their patients and their patients’
parents of the need to be immunized. In addition there is
evidence that vaccine messages that only target sexual
transmission of HPV reduce the probability that sexually
inexperienced, college age women will take the vaccine.28
The continual emphasis on the sexual transmissibility of
HPV has led to ignoring other potential routes of transmission. The genital focus of HPV dismisses the evidence
that HPV is found elsewhere in the body and in the environment. The emphasis on the vaccine in prevention of
cervical cancer overlooks evidence of other HPV-related
malignancies. Furthermore, providers have had to deal
with parental concerns about the safety of the vaccine. This
paper will discuss the scientific evidence related to each of
these issues.
Educating Patients and Parents
In counseling patients and their parents it is necessary to
desexualize the vaccine. Parents may raise the issue of: “If I
give my son/daughter the vaccine he/she will think it is o.k.
to have sex.” There are no data to support the notion that
vaccinated teens are more likely to have sex. Contrarily,
since the introduction of the vaccine in 2006, the number of
teens reporting that they have ever had sex and the number
stating that they have had 4 or more sexual partners has
remained constant.29 In a national probability sample of
1243 women ages 15-24, it was found that those who had
been given the HPV vaccine were not more likely to be
sexually active or to have more sex partners.10 However,
sexually active women who received the vaccine were 3
times more likely to always use a condom.9 Another study
R.M. Grimes et al. / J Pediatr Adolesc Gynecol 26 (2013) 243e248
showed that most adolescent females who received the
vaccine did not perceive that that they could cease practicing safe sex.30 Most recently, a study of over 1300 girls
found that the girls who received the vaccine at ages 11 to
12 were not more likely to have sexual activity-related
medical conditions. During a 3-year follow-up period, the
girls in this study who received the HPV vaccine were no
more likely to have infections with chlamydia, or a positive
pregnancy test.31 Women in their late teens or early
twenties may also say that they are not having sex so that
they do not need the vaccine. It should be pointed out to
these women that it is the ideal time to be immunized
before they have the chance to become infected and that
their current level of sexual activity is not likely to last for
the rest of their lives.
Parents may also raise the concern; “Why should I give
my child a vaccine to protect against a sexually transmitted
infection?” Patients in their late teens and early twenties
may raise the same question about themselves. Clinicians
must educate parents and patients that while HPV infection
can be sexually transmitted there are other ways that is
can be transmitted. Many studies have shown that HPV
is transmitted vertically, from mother to child. A metaanalysis of 9 studies involving 2113 mother infant pairs
showed a pooled risk of an HPV infected mother having an
infected infant was 24.3%. Two of the 9 studies in the metaanalysis looked for only HPV types 16 and 18 and these
studies revealed that 2.8% of infants born to mothers who
tested negative for HPV were found to be positive for HPV
types 16 or 18.32 Whether the transmission occurs in utero
or at the time of birth is not clear. A study from Brazil showed
that there was concordance between HPV types found in
cord blood or the placenta and the serotype that was found
in the infant after delivery.33 The previously mentioned
meta-analysis showed that infants who were vaginally
delivered were 1.8 times more likely to be infected. Apparently, transmission may take place either before or during
birth.32 There is also evidence that infants who are HPV
negative at birth are found to positive at older ages34 with 1
study showing that 136 and 116 infants acquired oral and
genital HPV respectively after having previously tested
negative.35 The route of transmission for this is not clear but
is presumably from touch of the mother, although HPV type
16 has also been found in breast milk,36 on nipples,37 and in
breast tissue.38,39 Whether HPV infections persist in children is not clear. A study of children who acquired HPV at
birth or infancy showed that it did persist for 26 months in
over 10% of the infected children.35 However, HPV was only
sought in the oral cavity and with genital swabs. So, it is
possible there could be other locations where the virus is
present or there could be a reservoir for these viruses elsewhere in the body. Further evidence of persistence of HPV in
children is found in a Swedish study of 1031 children aged
0 to 13 years in Stockholm. HPV seroprevalence among these
children was 3.0% for HPV16, 0.6% for HPV18, and 2.7% for
HPV33 (another oncogenic subtype).40 However, these
children may have cleared the virus but been re-infected
through contact with their parents.
The ability of either adults or children to clear the body of
HPV is not known. The research in this area is confounded
245
by whether prevalence is measured by examination of cells
recovered from various body locations, by actual recovery of
the virus itself or by the presence of antibodies. Recovery of
skin cells depends on the technique that is used, how
extensive the swabbing used in the cell recovery is and
which body sites are examined. Seroprevalence of antibodies may reflect infections that occurred recently or long
before. This is very useful in determining incidence but is
not necessarily a good measure of persistence of the virus.
A meta-analysis of persistence in cervical lesions from
studies of over 100,000 women showed that most women
who had normal cytology at baseline but developed
abnormal cytology subsequently managed to clear their
cervical HPV infections within a year or so with median
time of 12.4 months for HPV 16 and 9.8 months for HPV 18.
Follow up periods in the reviewed studies were relatively
short so it is not clear whether some HPV strains persist in
some women for extended periods of time or whether what
appears to be persistence merely reflects reinfection.41
A study of persistence of HPV in Danish male soldiers
used penile swabs on a periodic basis to examine persistence. It was found that 31 of 73 HPV infected men cleared
their HPV infections of the penis by 6 months after infection. However, most of these men were sexually active so
the failure to clear may also indicate re-infection.42 A study
of 1110 men from the United States, Mexico and Brazil used
polymerase chain reaction and genotypic testing for HPV in
the anus at baseline and 6 months later. Among men who
have sex with men (MSM), 41.7% were infected with at least
1 oncogenic HPV type during the course of the study. Men
who had sex with women (MSW) had a period prevalence
rate of 9.0%. Sixteen percent of MSM had at least 1 oncogenic type at the anal canal that was persistent from baseline to the 6-month visit. This was only 1.6% for MSW.43
However, it needs to be recognized that some of what
appear to be persistent cases may actually be reinfections.
So, it is possible that HPV does persist in adults although
these studies only examined genital areas. What appears to
be clearance in these subjects may only reflect the disappearance in the sampled sites. The potential for a reservoir
was found in a study that discovered that high risk HPV
types could be found in the vas deferens of men who
underwent vasectomies even though HPV could not be
found in semen sera.44
In study of 290 Finnish women who were followed for
36 months after their first post partum visit showed that
there was little decay in HPV 6, 11, 16, and 18 antibodies.
Seroprevalence of HPV 6, 11, 16, and 18 was 53.3, 21.5, 34.9,
and 21.5% at baseline and antibody decay was observed in
only 2.3, 4.0, 5.3, and 4.5% respectively in these women.
Decay time varied from 27.2 to 35.8 months. This may be due
to the persistence of the infection or due to the fact that they
were being constantly infected by their sexual partners. The
latter may be a more likely explanation in that HPV seroconversion rates during the period were 26.7% for HPV 6,
13.9% for HPV 11, 17.0% for HPV 16, and 16.8% for HPV 18.45
Finally it can be pointed out to parents that their child
has already been vaccinated against another virus that is
often sexually transmitted e hepatitis B. The hepatitis B
vaccine is given usually at birth and at 2 and 6 months of
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R.M. Grimes et al. / J Pediatr Adolesc Gynecol 26 (2013) 243e248
age. It was first made available for children in 1984;
however it did not become a routine part of the vaccine
schedule in the US until 1991. So, almost all pre-adolescents
have already been immunized against a virus that is sexually transmitted. Since 1991, rates of new hepatitis B infections have declined 82% in the United States. The decline has
been greatest among children born since 1991, when
routine vaccination of children was first recommended.46
Chronic hepatitis B infection is the cause of about 80% of
liver cancer worldwide with 1 study suggesting that
Hepatitis B surface Antigen (HBsAg) carriers have a 273-fold
higher risk of developing hepatocellular carcinoma.47 In
children, HBsAg is present in 100% of liver cancers. Taiwan
implemented routine HBV vaccination in 1984, and within
ten years child HBsAg carrier-rates declined from 10% to less
than 1%.48 Since vaccination of the infants has become the
standard, rates of hepatocellular cancer have declined 75%
in Taiwanese children 6-9 years old.49 Parents may also say
that; “My child is not having sex, why isn’t it o.k. to delay
vaccination until he/she is old enough to have intercourse?”
Parents may also argue that their daughters may never be
a risk for cervical cancer because they may not engage in
sexual activity until their marriage. Post-teen age women
may make the same argument. The educational demand in
this case is to point out that the vast majority of women are
not virgins at the time of their marriage. In addition, it is
highly unlikely that the person that they marry will be
a virgin and that perfect marital fidelity is an ideal but not
always a reality. This was illustrated by a study of 244
college women, all of whom were virgins at entry to the
study. After they began having sex with their first male
partner, 28.5% were HPV infected within a year and 50%
were infected within 3 years. The risk for HPV infection
increased if their partner had more lifetime partners.50
In educating patients and parents about HPV transmission, clinicians need to dispel the myth that pathogenic
HPV is only found on the genitals and in the anuses of men
and women who have had penetrating sex. There is abundant evidence that HPV can be found elsewhere on the body.
A recent study that collected specimens from a representative sample of Americans between the ages of 14 and 69
showed that HPV could be found in oral cavities of 6.9% of
the sample.51 A study of 128 female university students
demonstrated that HPV could be found on the fingertips of
nearly 30% of these women during a study period that
averaged 8 months.52 Another study found that 12 of 22
patients with genital warts also had similar HPV subtypes
on their fingertips.53 Pathogenic HPV has also been found in
eyebrow hairs,54 hair follicle samples taken from arms, legs,
scalps, and eyebrows,55 pubic hair,56 breast tissue,57 sinonasal areas,58 and nipples.37 Given that HPV is known to be
transmitted by skin to skin contact, non sexual transmission
is not only possible but quite likely. This is reinforced by an
Italian study which found genital warts in 88 women with
intact hymens who denied ever having sex.59
There is also the potential of transmission from objects in
the environment. Pathogenic strains of HPV have been
recovered from surfaces in a genitourinary medicine clinic
including examination lamps, treatment beds, and colposcope handles, cryoguns, and bed control switches.60 These
strains have likewise been recovered from light switches
and toilet seats in this clinic.61 HPV has also been
recovered from the underwear of HPV infected women.62
Furthermore, there is the potential of nosocomial infections resulting from improperly decontaminated medical
instruments including specula63 and ultrasound probes.64
HPV has a remarkable facility for surviving outside of the
body and being resistant to decontamination procedures.
Studies have shown that HPV can be recovered from
surfaces as long as 7 days after being planted there.65,66
Attempts to eradicate HPV with heat to 56 C for 1 hour or
use of ethylenediaminetetraacetic acid did not eliminate
HPV in all samples.66 Another study showed that cleaning
with a “general purpose neutral liquid detergent” and
water, or with a disinfecting detergent in 70% methylated
spirits did not eliminate the virus from all contaminated
surfaces.61 Another study attempting to eradicate HPV
samples from ultrasound probes using “standard disinfection” was also unable to eliminate HPV in all cases.66
A final area of education that needs to be done is to make
certain that genital cancers are not the only cancer that is
linked to HPV infection. It is true that HPV is associated with
approximately 11,500 cervical cancers, 500 vaginal, 1600
vulvar, and 400 penile cancers each year. However, HPV is
also strongly linked to approximately 4500 anal cancers
with about 2900 of them in women.67 Women who report
having had anal sex are more likely to get anal HPV infections but HPV infection is also found in the anal canal of
women who deny ever having anal sex. The latter may
acquire the infection due to contact with the scrotum
during vaginal sex68 as the scrotum is a common site for
infection with HPV.69 As a result, the HPV vaccine is now
approved for prevention of anal cancer and that fact can be
emphasized in educating patients and parents.
HPV is also linked to 7400 cases of oropharyngeal cancer
each year.67 HPV has been found in squamous cell skin
cancers at other locations on the body.70 The rate of
detection of various types of HPV in cutaneous squamous
cell cancers in immunocompetent patients has ranged from
27% to 70%.71 Other studies have shown a much higher rate
of oncogenic HPV types in skin tumors of individuals who
are immunosuppressed from HIV or post-transplant medications, suggesting a role for HPV in the etiology of these
tumors.72,73,74 These cancers have been found in the ungual
and periungual areas,75 toes,76 oral cancers,77 and the
prostate.78,79 HPV has also been found in breast cancer
tumors. A review of 20 studies from 19 different countries
showed rates of HPV being found in breast cancer tumors
that ranged from 0% to 86%.80 It is not clear whether the
presence of HPV is causative in any of these cancers but it is
intriguing that the virus is found so often in these tumors.
Another parental and patient concern is about the safety
of the vaccine. This concern may be linked to internet based
warnings about not taking the vaccine.81 However, these
warnings are not based on scientific data. The Center for
Disease Control and Prevention Vaccine Safety Datalinks’s
active surveillance looked at specific adverse events
following more than 600,000 doses of Gardasil. These
syndrome, stroke, venous
events were Guillain-Barre
thromboembolism, appendicitis, seizures, syncope, allergic
R.M. Grimes et al. / J Pediatr Adolesc Gynecol 26 (2013) 243e248
reactions, and anaphylaxis. No statistically significant
increased risk for any of these adverse events was detected
after vaccination. The CDC further reported that “Postlicensure safety monitoring from June 2006 through March
2012 continues to show no new HPV vaccine safety
concerns.”82 A review of 5 clinical studies compared 11,778
subjects who received at least 1 dose of the HPV vaccine to
9686 persons who received placebo injections. Serious
adverse events that occurred within 6 months of the
injections were found in 0.9%of those receiving the vaccine
vs 1.1%% in the placebo group. In addition, it was found that
other medical conditions were more likely to occur in the
placebo group.83 So, concerns about the safety of the
vaccine seem to be related to the cult beliefs about the
dangers of vaccines in general.
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Advocacy
Obtaining parental and patient acquiescence to receipt of
the vaccine can have a significant benefit to the patient and
is strongly impacted by the attending physician. One study
demonstrated that, if their physician strongly recommended the HPV vaccine, 19-26-year-old women were 3
times more likely to receive the vaccine than if the physician’s recommendation was lukewarm.84 Pediatricians need
to pre-empt and allay parental concerns about the vaccine
being an inducement to promiscuity and about the safety of
the vaccine when they advocate the vaccine. Clinicians who
are counseling their patients and the parents of their
patients about the importance of receiving the HPV vaccine
not only have to talk about the sexual nature of HPV transmission but also have to emphasize the potential for transmission from other forms of skin to skin contact and from
fomites. The discussion can also point out that there are
approximately as many non-genital cancers linked to HPV as
those associated with the cervix. In counseling patients, the
vaccine should be described as a protection against skin and
mucous membrane cancers and not just as protection
against a sexually transmitted infection because there are
more than sufficient data to believe that the infection can be
transmitted by non-sexual means. It is crucial that parents
and patients understand that this vaccine is more than
a preventer of sexually transmitted disease. For, until the
acceptance rate of the HPV vaccine becomes high enough to
reach a level where we achieve herd immunity, we will
never see the extraordinary reduction in transmitted HPV
infections that has been achieved by the Australians.
Acknowledgments
Preparation of this manuscript was partially supported
by the Baylor-UTHouston Center for AIDS Research (CFAR),
an NIH-funded program (AI036211), and NIH K12
(5KL2RR024149-05)
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